Strong Genome-Wide Selection Early in the Evolution of Prochlorococcus Resulted in a Reduced Genome through the Loss of a Large Number of Small Effect Genes

Abstract

The smallest genomes of any photosynthetic organisms are found in a group of free-living marine cyanobacteria, Prochlorococcus. To determine the underlying evolutionary mechanisms, we developed a new method to reconstruct the steps leading to the Prochlorococcus genome reduction using 12 Prochlorococcus and 6 marine Synechococcus genomes. Our results reveal that small genome sizes within Prochlorococcus were largely determined shortly after the split of Prochlorococcus and Synechococcus (an early big shrink) and thus for the first time decouple the genome reduction from Prochlorococcus diversification. A maximum likelihood approach was then used to estimate changes of nucleotide substitution rate and selection strength along Prochlorococcus evolution in a phylogenetic framework. Strong genome wide purifying selection was associated with the loss of many genes in the early evolutionary stage. The deleted genes were distributed around the genome, participated in many different functional categories and in general had been under relaxed selection pressure. We propose that shortly after Prochlorococcus diverged from its common ancestor with marine Synechococcus, its population size increased quickly thus increasing efficacy of selection. Due to limited nutrients and a relatively constant environment, selection favored a streamlined genome for maximum economy. Strong genome wide selection subsequently caused the loss of genes with small functional effect including the loss of some DNA repair genes. In summary, genome reduction in Prochlorococcus resulted in genome features that are similar to symbiotic bacteria and pathogens, however, the small genome sizes resulted from an increase in genome wide selection rather than a consequence of a reduced ecological niche or relaxed selection due to genetic drift.

Lack of Overt Genome Reduction in the Bryostatin-Producing Bryozoan Symbiont “Candidatus Endobugula sertula”

“…Reductive evolution is known to occur in a number of settings, including intracellular symbiosis (18,53), intracellular pathogenesis (54), and free-living pelagic microbes (55). In strictly intracellular organisms, reduction is thought to occur due to genetic drift as a consequence of genetic isolation and strict vertical transmission, low effective population sizes, and frequent bottlenecks (18).…”

Black Queen evolution: the role of leakiness in structuring microbial communities

“…First, the minimum effect size required for a mutation to be 'seen' by natural selection is inversely related to the effective population size. Therefore, even very small fitness benefits can be selected in the very large populations typical of freeliving microbes, allowing efficient 'streamlining' of genomes [2,76]. Second, microbes frequently gain new functions via HGT, but when first acquired these functions are poorly integrated into the pre-existing genome [77].…”

Endosymbiont evolution: predictions from theory and surprises from genomes

“…Free-living bacteria with small genomes discovered to date tend to live in nutrient-poor marine environments. Even cultured isolates can have small genomes, including strains of Prochlorococcus marinus (the abundant photosynthetic species with genomes as small as 1.64 Mb 116 ) and culturable members of SAR11, a diverse clade characterized by small (average 1.34 Mb), AT-rich genomes. 117, 118 Single-cell genomics of bacteria in oligotrophic environments have revealed that uncultured representatives have even smaller (e.g., an estimated 0.61 Mb for strain AAA076-M08 119 ) and, interestingly, more AT-rich genomes than related cultured isolates.…”

“…While diverse mechanisms may underlie genome reduction in free-living bacteria, 116 adaptation has been emphasized. Under a model of adaptive genome reduction, often phrased as genome streamlining , smaller genomes may be advantageous, particularly in nutrient-poor environments where fitness is determined by competition for scarce resources.…”